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Language Proficiency

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Language Proficiency Modulates the Recruitment ofNon-Classical Language Areas in BilingualsMatthew K. Leonard1,2*, Christina Torres2,3, Katherine E. Travis2,4, Timothy T. Brown2,4, Donald J.Hagler Jr.2,3, Anders M. Dale2,3,4, Jeffrey L. Elman1,5, Eric Halgren2,3,4,51 Department of Cognitive Science, University of California San Diego, La Jolla, California, United States of America, 2 Multimodal Imaging Laboratory, University ofCalifornia San Diego, La Jolla, California, United States of America, 3 Department of Radiology, University of California San Diego, La Jolla, California, United States ofAmerica, 4 Department of Neurosciences, University of California San Diego, La Jolla, California, United States of America, 5 Kavli Institute for Brain and Mind, University ofCalifornia San Diego, La Jolla, California, United States of AmericaAbstractBilingualism provides a unique opportunity for understanding the relative roles of proficiency and order of acquisition indetermining how the brain represents language. In a previous study, we combined magnetoencephalography (MEG) andmagnetic resonance imaging (MRI) to examine the spatiotemporal dynamics of word processing in a group of Spanish-English bilinguals who were more proficient in their native language. We found that from the earliest stages of lexicalprocessing, words in the second language evoke greater activity in bilateral posterior visual regions, while activity to thenative language is largely confined to classical left hemisphere fronto-temporal areas. In the present study, we sought toexamine whether these effects relate to language proficiency or order of language acquisition by testing Spanish-Englishbilingual subjects who had become dominant in their second language. Additionally, we wanted to determine whetheractivity in bilateral visual regions was related to the presentation of written words in our previous study, so we presentedsubjects with both written and auditory words. We found greater activity for the less proficient native language in bilateralposterior visual regions for both the visual and auditory modalities, which started during the earliest word encoding stagesand continued through lexico-semantic processing. In classical left fronto-temporal regions, the two languages evokedsimilar activity. Therefore, it is the lack of proficiency rather than secondary acquisition order that determines therecruitment of non-classical areas for word processing.Citation: Leonard MK, Torres C, Travis KE, Brown TT, Hagler DJ Jr, et al. (2011) Language Proficiency Modulates the Recruitment of Non-Classical Language Areasin Bilinguals. PLoS ONE 6(3): e18240. doi:10.1371/journal.pone.0018240Editor: Pedro Valdes-Sosa, Cuban Neuroscience Center, CubaReceived September 13, 2010; Accepted March 1, 2011; Published March 24, 2011Copyright: ß 2011 Leonard et al. This is an open-access article distributed under the terms of the Creative Commons Attrib ution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Funding: NSF grant BCS-0924539 (http://www.nsf.gov/), Innovative research grant from the Kavli Institute for Brain and Mind at UCSD (http ://kibm.ucsd.edu/),NIH grant R01 NS18741, NIH Training grant T32 MH20 002 to the UCSD Institute for Neural Computation, NIH Training grant T32 DC00041 to the UCSD Center forResearch in Language, NIH award K32 NS05609, and NIH grant HD53136 (http://www.nih.gov/). The funders had no role in study design, data collection andanalysis, decision to publish, or preparation of the manuscript.Competing Interests: The authors have declared that no competing interests exist.* E-mail: [email protected] is a fascinating and complex phenomenon ofculture, identity, and skill that deserves attention for itsprominence among modern societies and also for what it can tellus about language and cognitive ability more broadly. Previousstudies have shown that proficiency modulates lexico-semanticprocessing in both languages in bilinguals, as indexed by reactiontime priming tasks [1–4], electroencephalographic methods [5,6],and brain imaging studies [7–11]. The Revised HierarchicalModel (RHM) for bilingual language representation predicts thesefindings as arising from proficiency-modulated links between thefirst (L1) and second (L2) languages and a supramodal conceptualstore [12].It is unclear how these links are mediated in the neural systemsthat underlie word processing in the two languages and how theychange when one becomes more proficient in the second-learnedlanguage. In a previous study, we combined magnetoencephalog-raphy (MEG) and structural MRI to show that when readingwords in Spanish and English, native Spanish speakers who arestill dominant in Spanish have overlapping activity for bothlanguages in classical left fronto-temporal regions during lexico-semantic processing [13]. In contrast, activity to words in the lessproficient English additionally involves right hemisphere andbilateral secondary visual regions such as lateral and ventraloccipitotemporal cortex (LOT and VOT) as early as ,135 ms,and continuing through long latency time windows (,400 ms aftera word was shown). Furthermore, only less familiar words in theless familiar language showed this pattern, suggesting that theseregions may become active when the initial task of identifyingwords is more difficult [14,15]. Several imaging studies have foundmore distributed activity for the less proficient language [8,13,16–20], however this is a controversial interpretation [7].In the present study, we tested native Spanish speakers who hadbecome dominant in English to examine whether greater activityin non-classical language areas is associated with lower proficiency(where Spanish would evoke greater activity in LOT and VOT) ororder of acquisition (where English would evoke greater activity inthese areas, identical to our previous study). We also sought toexamine whether bilateral visual activity that occurs after sensory-perceptual processing is related to the visual paradigm we used inour previous study. Therefore, we presented subjects with words inPLoS ONE | www.plosone.org 1 March 2011 | Volume 6 | Issue 3 | e18240both the visual and auditory modalities to confirm that bilateralvisual activity in object processing regions like LOT is lexico-semantic in nature, and not tied to the stimulus modality. Wefound that although the


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